Post-transplantation cyclophosphamide is associated with increased bacterial infections.


Journal

Bone marrow transplantation
ISSN: 1476-5365
Titre abrégé: Bone Marrow Transplant
Pays: England
ID NLM: 8702459

Informations de publication

Date de publication:
31 Oct 2023
Historique:
received: 26 04 2023
accepted: 13 10 2023
revised: 05 10 2023
medline: 31 10 2023
pubmed: 31 10 2023
entrez: 31 10 2023
Statut: aheadofprint

Résumé

Post-transplant cyclophosphamide (PTCy) is increasingly used to reduce graft-versus-host disease after hematopoietic cell transplantation (HCT); however, it might be associated with more infections. All patients who were ≥2 years old, receiving haploidentical or matched sibling donor (Sib) HCT for acute leukemias or myelodysplastic syndrome, and either calcineurin inhibitor (CNI)- or PTCy-based GVHD prophylaxis [Haploidentical HCT with PTCy (HaploCy), 757; Sibling with PTCy (SibCy), 403; Sibling with CNI-based (SibCNI), 1605] were included. Most bacterial infections occurred within the first 100 days; 953 patients (34.5%) had at least 1 infection and 352 patients (13%) had ≥2 infections. Patients receiving PTCy had a greater incidence of bacterial infections by day 180 [HaploCy 46%; SibCy 48%; SibCNI 35%; p < 0.001]. Compared with the SibCNI without infection cohort, 1.99-fold, 3.33-fold, 2.78-fold, and 2.53-fold increased TRM was seen for the HaploCy cohort without infection and HaploCy, SibCy, and SibCNI cohorts with infection, respectively. Bacterial infections increased mortality [HaploCy (HR1.84, 99% CI: 1.45-2.33, p < 0.0001), SibCy cohort (HR,1.68, 99% CI: 1.30-2.19, p < 0.0001), and SibCNI cohort (HR,1.76, 99% CI: 1.43-2.16, p < 0.0001). PTCy was associated with increased bacterial infections regardless of donor, and bacterial infections were associated with increased mortality irrespective of GVHD prophylaxis. Patients receiving PTCy should be monitored carefully for bacterial infections following PTCy.

Identifiants

pubmed: 37903992
doi: 10.1038/s41409-023-02131-z
pii: 10.1038/s41409-023-02131-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NCI NIH HHS
ID : U24 CA076518
Pays : United States

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Vydra J, Shanley RM, George I, Ustun C, Smith AR, Weisdorf DJ, et al. Enterococcal bacteremia is associated with increased risk of mortality in recipients of allogeneic hematopoietic stem cell transplantation. Clin Infect Dis. 2012;55:764–70.
doi: 10.1093/cid/cis550 pubmed: 22693346 pmcid: 3657510
Ballen K, Woo Ahn K, Chen M, Abdel-Azim H, Ahmed I, Aljurf M, et al. Infection rates among acute leukemia patients receiving alternative donor hematopoietic cell transplantation. Biol Blood Marrow Transpl. 2016;22:1636–45.
doi: 10.1016/j.bbmt.2016.06.012
Papanicolaou GA, Ustun C, Young JH, Chen M, Kim S, Ahn KW, et al. Bloodstream infection (BSI) due to Vancomycin-Resistant Enterococcus (VRE) is associated with increased mortality after hematopoietic cell transplantation for acute leukemia and myelodysplastic syndrome: a multicenter, retrospective cohort study. Clin Infect Dis. 2019;69:1771–9.
Ustun C, Kim S, Chen M, Beitinjaneh AM, Brown VI, Dahi PB, et al. Increased overall and bacterial infections following myeloablative allogeneic HCT for patients with AML in CR1. Blood Adv. 2019;3:2525–36.
doi: 10.1182/bloodadvances.2019000226 pubmed: 31471322 pmcid: 6737406
Ustun C, Young JH, Papanicolaou GA, Kim S, Ahn KW, Chen M, et al. Bacterial blood stream infections (BSIs), particularly post-engraftment BSIs, are associated with increased mortality after allogeneic hematopoietic cell transplantation. Bone Marrow Transpl. 2019;54:1254–65.
doi: 10.1038/s41409-018-0401-4
Akhmedov M, Klyasova G, Kuzmina L, Fedorova A, Vasilyeva V, Drokov M, et al. Incidence, etiology, risk factors, and outcomes of pre-engraftment bloodstream infections after first and second allogeneic hematopoietic cell transplantation. Transpl Infect Dis. 2022;24:e13842.
doi: 10.1111/tid.13842 pubmed: 35501664
Dandoy CE, Kim S, Chen M, Ahn KW, Ardura MI, Brown V, et al. Incidence, risk factors, and outcomes of patients who develop mucosal barrier injury-laboratory confirmed bloodstream infections in the first 100 days after allogeneic hematopoietic stem cell transplant. JAMA Netw Open. 2020;3:e1918668.
doi: 10.1001/jamanetworkopen.2019.18668 pubmed: 31913492 pmcid: 6991246
Takagi S, Ogura S, Araoka H, Uchida N, Mitsuki T, Yuasa M, et al. The impact of graft cell source on bloodstream infection in the first 100 days after allogeneic hematopoietic cell transplantation. Bone Marrow Transpl. 2021;56:1625–34.
doi: 10.1038/s41409-021-01229-6
Dandoy CE, Ardura MI, Papanicolaou GA, Auletta JJ. Bacterial bloodstream infections in the allogeneic hematopoietic cell transplant patient: new considerations for a persistent nemesis. Bone Marrow Transpl. 2017;52:1091–106.
doi: 10.1038/bmt.2017.14
Nathan S, Ustun C. Complications of stem cell transplantation that affect infections in stem cell transplant recipients, with analogies to patients with hematologic malignancies. Infect Dis Clin North Am. 2019;33:331–59.
doi: 10.1016/j.idc.2019.01.002 pubmed: 30940464
Mielcarek M, Furlong T, O’Donnell PV, Storer BE, McCune JS, Storb R, et al. Posttransplantation cyclophosphamide for prevention of graft-versus-host disease after HLA-matched mobilized blood cell transplantation. Blood. 2016;127:1502–8.
doi: 10.1182/blood-2015-10-672071 pubmed: 26764356 pmcid: 4797026
Luznik L, O’Donnell PV, Symons HJ, Chen AR, Leffell MS, Zahurak M, et al. HLA-haploidentical bone marrow transplantation for hematologic malignancies using nonmyeloablative conditioning and high-dose, posttransplantation cyclophosphamide. Biol Blood Marrow Transpl. 2008;14:641–50.
doi: 10.1016/j.bbmt.2008.03.005
Saliba RM, Alousi AM, Pidala J, Arora M, Spellman SR, Hemmer MT, et al. Characteristics of Graft-Versus-Host Disease (GvHD) after post-transplantation cyclophosphamide versus conventional GvHD prophylaxis. Transpl Cell Ther. 2022;28:681–93.
doi: 10.1016/j.jtct.2022.07.013
McCurdy SR, Luznik L. How we perform haploidentical stem cell transplantation with posttransplant cyclophosphamide. Hematol Am Soc Hematol Educ Program. 2019;2019:513–21.
doi: 10.1182/hematology.2019001323
Webster JA, Luznik L, Tsai HL, Imus PH, DeZern AE, Pratz KW, et al. Allogeneic transplantation for Ph+ acute lymphoblastic leukemia with posttransplantation cyclophosphamide. Blood Adv. 2020;4:5078–88.
doi: 10.1182/bloodadvances.2020002945 pubmed: 33080006 pmcid: 7594402
Goldsmith SR, Slade M, DiPersio JF, Westervelt P, Lawrence SJ, Uy GL, et al. Cytomegalovirus viremia, disease, and impact on relapse in T-cell replete peripheral blood haploidentical hematopoietic cell transplantation with post-transplant cyclophosphamide. Haematologica. 2016;101:e465–e468.
doi: 10.3324/haematol.2016.149880 pubmed: 27443287 pmcid: 5394884
Huntley D, Gimenez E, Pascual MJ, Hernandez-Boluda JC, Gago B, Vazquez L, et al. Incidence, features, and outcomes of cytomegalovirus DNAemia in unmanipulated haploidentical allogeneic hematopoietic stem cell transplantation with post-transplantation cyclophosphamide. Transpl Infect Dis. 2020;22:e13206.
doi: 10.1111/tid.13206 pubmed: 31677215
Jamy O, Hebert C, Dunn-Valadez S, Magnusson T, Watts N, McGwin G, et al. Risk of cytomegalovirus infection with post-transplantation cyclophosphamide in haploidentical and hla-matched unrelated donor transplantation. Transplant Cell Ther. 2022;28:213.e1-213.e6.
Goldsmith SR, Abid MB, Auletta JJ, Bashey A, Beitinjaneh A, Castillo P, et al. Posttransplant cyclophosphamide is associated with increased cytomegalovirus infection: a CIBMTR analysis. Blood. 2021;137:3291–305.
doi: 10.1182/blood.2020009362 pubmed: 33657221 pmcid: 8351903
Singh A, Dandoy CE, Chen M, Kim S, Mulroney CM, Kharfan-Dabaja MA, et al. Post-transplantation cyclophosphamide is associated with an increase in non-cytomegalovirus herpesvirus infections in patients with acute leukemia and myelodysplastic syndrome. Transp Cell Ther. 2022;28:48. e41–48.e10.
Mulroney CM, Abid MB, Bashey A, Chemaly RF, Ciurea SO, Chen M, et al. Incidence and impact of community respiratory viral infections in post‐transplant cyclophosphamide‐based graft‐versus‐host disease prophylaxis and haploidentical stem cell transplantation. Br J Haematol. 2021;194:145–57.
doi: 10.1111/bjh.17563 pubmed: 34124796 pmcid: 8853845
Esquirol A, Pascual MJ, Kwon M, Pérez A, Parody R, Ferra C, et al. Severe infections and infection-related mortality in a large series of haploidentical hematopoietic stem cell transplantation with post-transplant cyclophosphamide. Bone Marrow Transpl. 2021;56:2432–44.
doi: 10.1038/s41409-021-01328-4
Mikulska M, Raiola AM, Galaverna F, Balletto E, Borghesi ML, Varaldo R, et al. Pre-engraftment bloodstream infections after allogeneic hematopoietic cell transplantation: impact of T cell-replete transplantation from a haploidentical donor. Biol Blood Marrow Transpl. 2018;24:109–18.
doi: 10.1016/j.bbmt.2017.08.024
Oltolini C, Greco R, Galli L, Clerici D, Lorentino F, Xue E, et al. Infections after allogenic transplant with post-transplant cyclophosphamide: impact of donor HLA matching. Biol Blood Marrow Transpl. 2020;26:1179–88.
doi: 10.1016/j.bbmt.2020.01.013
manual Cfi. Q428- 440: infection. 2020; Available from: https://www.cibmtr.org/manuals/fim/1/en/topic/f2100-q428-440 Accesed 5 Mar 2022.
Tomblyn M, Young JA, Haagenson MD, Klein JP, Trachtenberg EA, Storek J, et al. Decreased infections in recipients of unrelated donor hematopoietic cell transplantation from donors with an activating KIR genotype. Biol Blood Marrow Transpl. 2010;16:1155–61.
doi: 10.1016/j.bbmt.2010.02.024
See I, Iwamoto M, Allen-Bridson K, Horan T, Magill SS, Thompson ND. Mucosal barrier injury laboratory-confirmed bloodstream infection: results from a field test of a new National Healthcare Safety Network definition. Infect Control Hosp Epidemiol. 2013;34:769–76.
doi: 10.1086/671281 pubmed: 23838215
Epstein L, See I, Edwards JR, Magill SS, Thompson ND. Mucosal Barrier Injury Laboratory-Confirmed Bloodstream Infections (MBI-LCBI): descriptive analysis of data reported to National Healthcare Safety Network (NHSN), 2013. Infect Control Hosp Epidemiol. 2016;37:2–7.
doi: 10.1017/ice.2015.245 pubmed: 26456954
Kim S, Logan B, Riches M, Chen M, Ahn KW. Statistical methods for time-dependent variables in hematopoietic cell transplantation studies. Transpl Cell Ther. 2021;27:125–32.
doi: 10.1016/j.bbmt.2020.09.034
Commenges D, Andersen PK. Score test of homogeneity for survival data. Lifetime Data Anal. 1995;1:145–56.
doi: 10.1007/BF00985764 pubmed: 9385097
Crocchiolo R, Bramanti S, Vai A, Sarina B, Mineri R, Casari E, et al. Infections after T-replete haploidentical transplantation and high-dose cyclophosphamide as graft-versus-host disease prophylaxis. Transpl Infect Dis. 2015;17:242–9.
doi: 10.1111/tid.12365 pubmed: 25648539 pmcid: 7169814
Fayard A, Daguenet E, Blaise D, Chevallier P, Labussiere H, Berceanu A, et al. Evaluation of infectious complications after haploidentical hematopoietic stem cell transplantation with post-transplant cyclophosphamide following reduced-intensity and myeloablative conditioning: a study on behalf of the Francophone Society of Stem Cell Transplantation and Cellular Therapy (SFGM-TC). Bone Marrow Transpl. 2019;54:1586–94.
doi: 10.1038/s41409-019-0475-7
Slade M, Goldsmith S, Romee R, DiPersio JF, Dubberke ER, Westervelt P, et al. Epidemiology of infections following haploidentical peripheral blood hematopoietic cell transplantation. Transpl Infect Dis. 2017;19:e12629.
Irene GC, Albert E, Anna BV, Rahinatu A, Silvana N, Silvana S, et al. Patterns of infection and infectious-related mortality in patients receiving post-transplant high dose cyclophosphamide as graft-versus-host-disease prophylaxis: impact of HLA donor matching. Bone Marrow Transpl. 2021;56:818–27.
doi: 10.1038/s41409-020-01092-x
Nagler A, Labopin M, Houhou M, Aljurf M, Mousavi A, Hamladji RM, et al. Outcome of haploidentical versus matched sibling donors in hematopoietic stem cell transplantation for adult patients with acute lymphoblastic leukemia: a study from the acute leukemia working party of the european society for blood and marrow transplantation. J Hematol Oncol. 2021;14:53.
doi: 10.1186/s13045-021-01065-7 pubmed: 33794963 pmcid: 8017786
Khimani F, Ranspach P, Elmariah H, Kim J, Whiting J, Nishihori T, et al. Increased infections and delayed CD4(+) T Cell but Faster B Cell immune reconstitution after post-transplantation cyclophosphamide compared to conventional GVHD prophylaxis in allogeneic transplantation. Transpl Cell Ther. 2021;27:940–8.
doi: 10.1016/j.jtct.2021.07.023
Salas MQ, Charry P, Puerta-Alcalde P, Martinez-Cibrian N, Solano MT, Serrahima A, et al. Bacterial bloodstream infections in patients undergoing allogeneic hematopoietic cell transplantation with post-transplantation cyclophosphamide. Transplant Cell Ther. 2022;28:850.e1-850.e10.
Ciurea SO, Mulanovich V, Saliba RM, Bayraktar UD, Jiang Y, Bassett R, et al. Improved early outcomes using a T cell replete graft compared with T cell depleted haploidentical hematopoietic stem cell transplantation. Biol Blood Marrow Transpl. 2012;18:1835–44.
doi: 10.1016/j.bbmt.2012.07.003
Holtan SG, Hamadani M, WU J, AL Malki MM, Runaas L, Elmariah H, et al. Post-transplant cyclophosphamide, tacrolimus, and mycophenolate mofetil as the new standard for Graft-Versus-Host Disease (GVHD) prophylaxis in reduced intensity conditioning: results from phase III BMT CTN 1703. Blood. 2022;140:LBA-4–LBA-4.
doi: 10.1182/blood-2022-171463

Auteurs

Celalettin Ustun (C)

Division of Hematology/Oncology/Cell Therapy, Rush University, Chicago, IL, USA. Celalettin_Ustun@rush.edu.

Min Chen (M)

CIBMTR® (Center for International Blood and Marrow Transplant Research), Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, USA.

Soyoung Kim (S)

CIBMTR® (Center for International Blood and Marrow Transplant Research), Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, USA.
Division of Biostatistics, Institute for Health and Equity, Medical College of Wisconsin, Milwaukee, WI, USA.

Jeffery J Auletta (JJ)

CIBMTR® (Center for International Blood and Marrow Transplant Research), National Marrow Donor Program/Be The Match, Minneapolis, MN, USA.
Hematology/Oncology/BMT and Infectious Diseases, Nationwide Children's Hospital, Columbus, OH, USA.

Marjorie V Batista (MV)

A.C. Camargo Cancer Center, Sao Paulo, Brazil.

Minoo Battiwalla (M)

Sarah Cannon Transplant and Cell Therapy Network, Nashville, TN, USA.

Jan Cerny (J)

Division of Hematology/Oncology, Department of Medicine, University of Massachusetts Chan Medical School and Medical Center, Worcester, MA, USA.

Lohith Gowda (L)

Yale Cancer Center and Yale School of Medicine, New Haven, CT, USA.

Joshua A Hill (JA)

Fred Hutchinson Cancer Center, Seattle, WA, USA.
University of Washington School of Medicine, Seattle, WA, USA.

Hongtao Liu (H)

Section of Hematology/Oncology, University of Chicago Medicine, Chicago, IL, USA.

Pashna N Munshi (PN)

Stem Cell Transplant and Cellular Immunotherapy Program, MedStar Georgetown University Hospital, Washington, DC, USA.

Sunita Nathan (S)

Division of Hematology/Oncology/Cell Therapy, Rush University, Chicago, IL, USA.

Matthew D Seftel (MD)

Department of Medicine, University of British Columbia, Vancouver, Canada.

John R Wingard (JR)

Division of Hematology & Oncology, Department of Medicine, University of Florida, Gainesville, FL, USA.

Roy F Chemaly (RF)

The University of Texas, M.D. Anderson Cancer Center, Houston, TX, USA.

Christopher E Dandoy (CE)

Cincinnati Children's Hospital Medical Center, University of Cincinnati School of Medicine, Cincinnati, OH, USA.

Miguel-Angel Perales (MA)

Adult Bone Marrow Transplant Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Department of Medicine, Weill Cornell Medical College, New York, NY, USA.

Marcie Riches (M)

CIBMTR® (Center for International Blood and Marrow Transplant Research), Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, USA.

Genovefa A Papanicolaou (GA)

Department of Medicine, Weill Cornell Medical College, New York, NY, USA.
Infectious Diseases Service, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Classifications MeSH